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A Practical Introduction to Stable-Isotope Analysis for Seabird Biologists: Approaches, Cautions and Caveats

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A Practical Introduction to Stable-Isotope Analysis for Seabird Biologists: Approaches, Cautions and Caveats Bond & Jones: Stable-isotopeForum analysis for seabird biologists 183 A PRACTICAL INTRODUCTION TO STABLE-ISOTOPE ANALYSIS FOR SEABIRD BIOLOGISTS: APPROACHES, CAUTIONS AND CAVEATS ALEXANDER L. BOND & IAN L. JONES Department of Biology, Memorial University of Newfoundland, St. John’s, Newfoundland and Labrador, A1B 3X9, Canada ([email protected]) Received 21 May 2008, accepted 15 March 2009 SUMMARY BOND, A.L. & JONES, I.L. 2009. A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Marine Ornithology 37: 183–188. Stable isotopes of carbon and nitrogen can provide valuable insight into seabird diet, but when interpreting results, seabird biologists need to recognize the many assumptions and caveats inherent in such analyses. Here, we summarize the most common limitations of stable-isotope analysis as applied to ecology (species-specific discrimination factors, within-system comparisons, prey sampling, changes in isotopic ratios over time and biological or physiological influences) in the context of seabird biology. Discrimination factors are species specific for both the consumer and the prey species, and yet these remain largely unquantified for seabirds. Absolute comparisons across systems are confounded by differences in the isotopic composition at the base of each food web, which ultimately determine consumer isotopic values. This understanding also applies to applications of stable isotopes to historical seabird diet reconstruction for which historical prey isotopic values are not available. Finally, species biology (e.g. foraging behaviour) and physiologic condition (e.g. level of nutritional stress) must be considered if isotopic values are to be interpreted accurately. Stable-isotope ecology is a powerful tool in seabird biology, but its usefulness is determined by the ability of scientists to interpret its results properly. Key words: δ13C, δ15N, assumptions, diet reconstruction, mixing model, seabird, stable isotopes INTRODUCTION Isotopic ratios are expressed as a parts-per-thousand difference in the ratio of the heavier (more rare) to the lighter (more common) Stable-isotope ratio analysis is now commonly used by seabird isotope (i.e. 13C to 12C), compared with the ratio found in an biologists to infer diet and trophic relationships, to gain insight international standard (Pee Dee Belemnite for carbon, atmospheric into the foraging ecology of species, and to inform population air for nitrogen) such that management (Inger & Bearhop 2008). First recognized in the mid- 1980s (Peterson & Fry 1987), the use of stable-isotope analysis in avian ecology became widespread only after a series of experiments , [1] and field studies in the early 1990s (Hobson & Clark 1992a, 1992b, where δX is either δ13C or δ15N, and R is either the ratio 13C/12C or 1993; Hobson et al. 1994). However, as early as 1997, concerns 15N/14N. were raised about untested assumptions of the properties of stable isotopes and a lack of controlled laboratory experiments (Gannes et The value of δ15N increases predictably with increasing trophic al. 1997). Since then, considerable advances have been made (Wolf level, because 14N is excreted preferentially in nitrogenous waste et al. 2009), although in a recent thorough review of seabird diet (Steele & Daniel 1978, Minagawa & Wada 1984, Kelly 2000). studies and methods (Barrett et al. 2007), stable-isotope analysis The carbon ratio also changes, but in smaller amounts, and only was the sole common method for which biases and drawbacks were at lower trophic levels (DeNiro & Epstein 1978, Rau et al. 1983, not discussed thoroughly. As a result, seabird biologists who wish Hobson & Welch 1992). Moreover, carbon exhibits a gradient, to use stable-isotope analysis face a daunting and often massive with inshore food sources being enriched in 13C as compared with task to navigate the conflicting papers and knowledge gaps in the offshore sources in the marine environment (Peterson & Fry 1987, scientific literature. Considerable gaps remain in our knowledge Kelly 2000). Carbon can therefore potentially act as a geographic of how elemental isotopes behave in biological systems, and little identifier (Quillfeldt et al. 2005). controlled experimentation has been conducted. Here, we present an introduction to stable-isotope analysis for seabird biologists new to Isotopic ratios are determined at the time of tissue synthesis in the this emerging, yet widespread, tool. For brevity, we discuss only the consumer (Hobson & Clark 1992a) and therefore offer themselves isotopes commonly used in seabird studies: carbon and nitrogen. to non-destructive sampling in live animals (i.e. blood, feathers, Marine Ornithology 37: 183–188 (2009) 184 Bond & Jones: Stable-isotope analysis for seabird biologists claws). These ratios can provide insight into seabird biology away such as muscle, liver and egg yolks almost certainly require lipid from the breeding colony if the proper tissue (e.g. moulted feathers) correction (Kojadinovic et al. 2008). is sampled. Tissue preservation DISCUSSION For many field studies, especially those involving seabirds on Lipids remote islands, the issue of tissue-preservation effects is of paramount importance. Formalin and genetic buffers can alter Compared with carbohydrates, lipids have less 13C because stable-isotope ratios drastically (Hobson et al. 1997, Gloutney & of fractionation caused by the oxidation of pyruvate to acetyl Hobson 1998), and results were mixed when tissues were preserved coenzyme A during lipid synthesis (DeNiro & Epstein 1977). in ethanol (Kaehler & Pakhomov 2001, Barrow et al. 2008). For Nevertheless, some researchers have found significant effects of avian tissue, freezing is the preferred method, but freezing may not lipid content on δ13C; others have not (McConnaughey & McRoy always be practical in the field, and so air drying (especially for 1979, Hobson & Clark 1992b, Pinnegar & Polunin 1999). blood samples) using an oven or similar smokeless heat source is also feasible (Bugoni et al. 2008). For a comprehensive review of Traditionally, lipids were removed from lipid-heavy tissues (C:N preservation techniques for stable-isotope samples, we direct the > 4.0) chemically (e.g. Bligh & Dyer 1959) to reduce variation reader to Barrow et al. (2008). in the isotopic ratio, but chemical extraction can also affect δ15N values (Murry et al. 2006). Two recent reviews (Post et al. 2007, Discrimination factors Logan et al. 2008) compared mathematical modelling methods and chemical extraction techniques, and concluded that analysing As prey nutrients are incorporated into the consumer, the isotopic a subset of samples before and after chemical lipid extraction will ratio changes by a “discrimination factor” (also called a “fractionation allow researchers to develop unique mathematical lipid models that factor”). In general, this factor falls between 0‰ and 2‰ for δ13C, can be applied to the remainder of the data in a given study. and between 2‰ and 5‰ for δ15N (Peterson & Fry 1987, Kelly 2000), and evidence is increasing that these ratios are unique to Seabird tissues such as feathers and egg albumen do not require each tissue–consumer–prey combination (Bearhop et al. 2002, lipid extraction (Kojadinovic et al. 2008), and blood typically does Cherel et al. 2005b, Caut et al. 2009). In addition, discrimination not. However, some Procellariiformes may have lipid-rich blood factors have long been regarded as an important aspect of stable- that would require lipid correction (Bond et al. 2010). Tissues isotope ecology (Mizutani et al. 1992) and are often applied poorly TABLE 1 Published mean discrimination factors for carbon and nitrogen stable isotopic ratios in seabird tissues based on a lipid-free fish dieta Species Consumer Discrimination factor (‰) Reference tissue C N King Penguin Aptenodytes patagonicus Whole blood –0.81 +2.07 Cherel et al. 2005b Feathers +0.07 +3.49 Cherel et al. 2005b Humboldt Penguin Spheniscus humboldtib Feathers +2.9 +4.8 Mizutani et al. 1992 Rockhopper Penguin Eudyptes chrysocome Whole blood +0.02 +2.72 Cherel et al. 2005b Feathers +0.11 +4.4 Cherel et al. 2005b Great Cormorant Phalacrocorax carbob Feathers +3.8 +3.7 Mizutani et al. 1992 Great Skua Stercorarius skua Whole blood +1.1 +2.8 Bearhop et al. 2002 Feathers +2.1 +4.6 Bearhop et al. 2002 Ring-billed Gull Larus delawarensis Whole blood –0.3 +3.1 Hobson & Clark 1992b Liver –0.4 +2.7 Hobson & Clark 1992b Muscle +0.3 +1.4 Hobson & Clark 1992b Bone collagen +2.6 +3.1 Hobson & Clark 1992b Feathers +0.2 +3.0 Hobson & Clark 1992b Black-tailed Gull L. crassirostrisb Feathers +5.3 +3.6 Mizutani et al. 1992 Common Murre Uria aalge Feather +1.2 +3.6 Becker et al. 2007 Rhinoceros Auklet Cerorhinca monocerata Whole blood — +3.49 Sears et al. 2009 a No discrimination factors have been published for members of the Diomedeidae, Procellariidae, Pelecanoididae, Hydrobatidae, Phaethontidae, Pelecanidae, Fregatidae, Sulidae or Rhyncopidae, or for other diets. b Lipids not extracted from prey items. Lipids result in a lower δ13C value, and therefore can change discrimination factors significantly. Marine Ornithology 37: 183–188 (2009) Bond & Jones: Stable-isotope analysis for seabird biologists 185 (Caut et al. 2009). A recent review by Caut et al. (2009) provided their isotope signatures reflect the diet during the period of growth a decision tree for approximating discrimination factors for avian (Hobson & Clark 1992a). Therefore, a diet comparison across tissues, but we urge
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